Microbial metabolism of electrons that are not associated with a chemical element, that is, ‘free’ electrons, is an intriguing metabolic capacity that has been primarily investigated in insoluble metal-reducing microorganisms, such as Shewanella or Geobacter species (Bond and Lovley (2003) Appl. Environ. Microbiol. 69:1548-1555; Hartshorne et al. (2009) Proc. Natl. Acad. Sci. USA 106:22169-22174; Coursolle et al. (2010) J. Bacteriol. 192:467-474; Clarke et al. (2011) Proc. Natl. Acad. Sci. USA 108:9384-9389; Lovley (2012) Annu. Rev. Microbiol. 66:391-409; Liu et al. (2014) Environ. Microbiol. Rep. 6:776-785; Malvankar and Lovley (2014) Curr. Opin. Biotechnol. 27C:88-95; Pirbadian et al. (2014) Proc. Natl. Acad. Sci. USA 111:12883-12888; TerAvest et al. (2014) Chemelectrochem. 1:1874-1879. In addition to these anodic microbial processes, recent studies have revealed that some microorganisms can take up ‘free’ cathodic electrons from conductive minerals during interspecies electron transfer (Kato et al. (2012) Proc. Natl. Acad. Sci. USA 109:10042-10046) or from abiotically reduced surfaces such as deep sea hydrothermal vent chimneys (Nakamura et al. (2010) Angew Chem. Int. Ed. Engl. 49:7692-7694). This use of ‘free’ electrons as electron donors in microbial catabolism also finds relevance in engineered bioelectrochemical systems, which have been emerging as promising platforms for a sustainable energy landscape. In particular, biocathodes in microbial electrosynthesis reactors are of interest, where microorganisms at the cathode convert electricity plus CO2 into useful chemical products. From a fundamental perspective, the mechanisms involved in cathodic electron uptake are most intriguing, however, largely unknown.
The most basic biocathode is the hydrogen-evolving bio-cathode. Most studies on hydrogen-evolving bio-cathodes in a microbial electrosynthesis reactor have been carried out using mixed microbial cultures (Jafary et al. (2015) Renew. Sust. Energ. Rev. 47:23-33), and the ecology of the different microorganisms in a community is poorly understood. A few studies showed hydrogen formation by pure cultures of Geobacter sulfurreducens (Geelhoed et al. (2010) Curr. Opin. Microbiol. 13:307-315) or Desulfovibrio species (Croese et al. (2011) Appl. Microbiol. Biotechnol. 92:1083-1093); Aulenta et al. (2012) Chemsuschem. 5:1080-1085), and the molecular mechanism of the electron uptake reaction in most hydrogen-evolving, biocathodic microorganisms is unknown (Jafary et al., supra).
A more specialized type of biocathode is found in microbial electro-synthesis. In this process, microorganisms convert cathode-derived electrons plus CO2 into organic compounds rather than free molecular hydrogen. Electrosynthetic methane formation has been achieved using mixed cultures (Cheng et al. (2009) Environ. Sci. Technol. 43:3953-3958, Siegert et al. (2015) ACS Sustain. Chem. Eng. 3:1668-1676) or pure strains such as Methanococcus maripaludis and Methanobacterium sp. (Lohner et al. (2014) ISME J. 8:1673-1681; Beese-Vasbender et al. (2015) Bioelectrochemistry 102:50-55). Multi-carbon compounds such as acetate have been synthesized on biocathodes using a diversity of homoacetogenic strains (Nevin et al. (2010) MBio 1:e00103-e00110, Nevin et al. (2011) Appl. Environ. Microbiol. 77:2882-2886, Deutzmann et al. (2015) Mbio 6:e00496-15).
Low electron transfer rates from the cathode during microbially catalyzed electrosynthesis were generally considered to be limiting the feasibility of this process on a commercial scale (Blanchet et al. (2015) Energ. Environ. Sci. 8:3731-3744). Moreover, overpotentials of 4200 mV had to be applied repeatedly to achieve significant electron transfer rates (Villano et al. (2010) Bioresour. Technol. 101:3085-3090, Aulenta et al. (2012) Chemsuschem. 5:1080-1085). At these low potentials, the electrochemical formation of small reduced molecules as potential electron carriers such as H2, CO or formate at the cathode cannot be excluded (Villano et al., supra; Yates et al. (2014) Int. J. Hydrogen Energ. 39:16841-16851; Deutzmann et al., supra). To our knowledge, all methanogens and homoacetogens studied for their electrosynthetic properties are able to metabolize at least some of these small reduced molecules.
Besides methanogenic archaea and homoacetogenic bacteria, Fe(0)-corroding microorganisms have been intensively investigated for their outstanding electron transfer capabilities (Dinh et al. (2004) Nature 427:829-832; Uchiyama et al. (2010) Appl. Environ. Microbiol. 76:1783-1788; Enning et al. (2012) Environ. Microbiol. 14:1772-1787; Venzlaff et al. (2013) Corros. Sci. 66: 88-96; Enning and Garrelfs (2014) Appl. Environ. Microbiol. 80:1226-1236; Kato et al. (2015) Appl. Environ. Microbiol. 81:67-73; Beese-Vasbender et al. (2015) Electrochimica Acta 167:321-329). Although direct electron uptake has been proposed in these microorganisms, no mechanism has been identified to date (Enning et al. (2012) Environ. Microbiol. 14:1772-1787; Venzlaff et al. (2013) Corros. Sci. 66:88-96; Enning and Garrelfs, supra; Beese-Vasbender et al. (2015) Electrochimica Acta 167:321-329). Recently, Fe(0)-corroding microorganisms, in particular strain IS4 (‘Desulfopila corrodens’, previously named Desulfobacterium corrodens (Dinh et al. (2004) Nature 427:829-832), have been investigated in electrode systems, and a direct electron transfer mechanism has been postulated (Venzlaff et al., supra; Beese-Vasbender et al. (2015) Electrochimica Acta 167:321-329).
There remains a need for developing better more efficient methods of utilizing microbial electrosynthesis to produce valuable compounds of economic interest.